Background

Ascaris lumbricoides, which causes ascariasis, is the largest of the round worms (nematodes), with females measuring 30 cm x 0.5 cm. It is present in the GI tract (small intestine) of 1.2–1.5 billion individuals in tropical and subtropical areas, making it the most common nematode infection in the world. The number of cases in the United States is estimated to be 4 million, with transmission occurring in the Gulf States and southern New Mexico and southern Arizona. See the image below.

The parasite is acquired through ingestion of embryonated eggs. Ascariasis is usually asymptomatic but can be complicated by several conditions, including appendicitis, bowel perforation, cholecystitis, intestinal obstruction (large numbers), malabsorption (eg, lactose, nitrogen, vitamin A), and pancreatitis. The mortality rate is 5% if complications occur. When the parasite migrates through the lung early in its parasitic cycle, it can also cause pneumonitis. The mainstays of chemotherapy include albendazole, mebendazole, and pyrantel pantoate (for alternatives, see Medication).

A lumbricoides is one of the soil-transmitted helminths (STH), a group that includes 16 worms. Many individuals are infected with 2-3 of the 3 major parasites (ie, A lumbricoides, Trichuris trichiura, and hookworm).

By chronically infecting school-aged children, usually in developing countries, these parasites significantly contribute to cognitive deficits, growth stunting, mental retardation, and malnutrition. The 3 most important infections are ascariasis (A lumbricoides) , trichuriasis (T trichiura), and hookworm (N americanus and A duodenale); often, all 3 parasites can be found in a single individual. The combined disease burden of the STHs is estimated to be equivalent to malaria or tuberculosis.

Although A lumbricoides has been present in humans for many thousands of years, science only began to elucidate its biology in the 17th century, and effective chemotherapy was only developed in the late 20th century. The earliest recovered eggs are from the 30,000-year-old Upper-Paleolithic site of Arcy-sur-Cure in Yonne, France. Infertile eggs have been reported in coprolites dating to 2277 BCE from an archeological site at Los Gavilanes, Peru. Desiccated human feces from Big Bone Cave, Tennessee dating to approximately 2177 BCE contained A lumbricoides. In the Nubian aspect of the Nile River, eggs have been recovered inside a mummy dating to 2050-1750 BCE.

In 1683, Tyson discussed " Lumbricus teres …observations on the Round Worm bred in human bodies….that common Round Worm which children u[s]ually are troubled with." In 1758, Linnaeus proposed the name Ascaris lumbricoides. In 1856, Ransom reported that finding eggs in fecal samples was a reliable means of diagnosis. In 1862, Davaine concluded that ingested embryonated eggs produced ascariasis and that the infected host would produce eggs in feces that could pass the infection to another host. In the 1980s, several reviews noted the public health impact of STH infection and suggested control strategies using antihelminthic drugs, some of which were introduced in the 1960s (eg, pyrantel pantoate) and 1970s (eg, mebendazole).

The genus Ascaris is composed of 17 species. A lumbricoides has a high host specificity for humans and, rarely, for pigs. It has been reported in other hosts, including cats, chimpanzees, domestic dogs, gibbons, gorillas, guinea-pigs, lambs, macaques, monkeys, rabbits, rats, and squirrels; however, it has not been demonstrated to achieve sexual maturity or to produce fertile eggs in these hosts.

Ascaris suum has a high host specificity for domestic pigs and, rarely, humans. It has been reported in other hosts, including domestic cattle, gorillas, goats, lambs, monkeys, mice, rabbits, and rats. As with A lumbricoides, A suum has not been demonstrated to achieve sexual maturity or to produce fertile eggs in these hosts. The other 15 species of Ascaris are not reported in humans. Therefore, A lumbricoides does not have an animal reservoir.

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Pathophysiology

Species in the genus Ascaris are transmitted via the fecal-oral route, primarily from ingestion of agricultural products or food contaminated with parasite eggs.

Life cycle

Life cycle data come from investigations of A suum in pigs and A lumbricoides in mice. Little is known about the interaction of A lumbricoides larvae and humans.

Humans ingest A lumbricoides eggs, which contain stage 2 larvae and measure 50-70 µm x 40-50 µm. The eggs hatch in the jejunum and release the stage 2 larvae. They then penetrate the small intestinal wall (some evidence suggests the large intestine), enter the portal venous circulation, and migrates to the liver over 2-8 days. According to data from mice, they measure 258 µm x 14 µm at this stage.

The larvae then migrate via the venous circulation to the pulmonary circulation and to the lungs. Here, the larvae measure 564 µm x 28 µm. They then break into the alveolar spaces, molt to the stage 3 larvae, grow to 1,700–2,000 µm, and molt to stage 4 larva, all over 4-14 days. They then ascend the trachea, are swallowed, return to the small intestine (usually intestine), molt for the final time, and develop into mature adults, all over 14-20 days. The total elapsed time in humans from the time of ingestion to development of mature adults is 18-42 days.

The size range of the mature female is 20-40 cm x 0.5–0.6 cm; the mature male is somewhat smaller at 12-25 cm x 0.3-0.4 cm. The Ascaris genus contains the largest of the nematode parasites; the migration through the tissues appears to confer this size advantage. In general, alimentary tract nematodes (700 species) that migrate through tissues grow faster.

Females produce approximately 200,000 eggs per day (134,462-358,750), although this number fluctuates. In the presence of a male, the eggs are fertilized by copulation. Female-only infections produce nonfertilized eggs that cannot become infective. Male-only infections produce no eggs. The prepatent period (time from ingestion of the egg to detection of the eggs in feces) is 67-76 days (67 d in children < 4 y). A suum infections in humans have a similar life cycle, with a prepatent period of 24-29 days.

The life span of A lumbricoides is 1-2 years. Eggs, fertilized and unfertilized, are released to the environment via feces. Unfertilized eggs do not become infective. Fertilized eggs cannot infect until they embryonate outside the human body under proper conditions. Fertile eggs have 4 layers. The outer layer, which is not always present, consists of an extruded, sticky mucopolysaccharide from the parent female worm. This provides adhesiveness thought to be advantageous, allowing the eggs to stick to many types of surfaces. The other 3 layers are secreted by the embryo and include an outer thin proteinaceous membrane, a middle protein and chitin layer that provides structural strength, and the inner ascaricide layer, which consists of protein (25%) and unsaponifiable lipid (75%). This inner ascaroside layer is selectively permeable and is important for the survival of the egg in various conditions.

To become infective, eggs must complete embryonization while in the soil. The zygote develops into a stage 1 larva and molts to a stage 2 larva within the egg shell. This occurs over 10-14 days at 28-32°C (82.4-89.6°F) and over 45-55 days at 16-18°C (60.8-64.4°F). Several factors favor survival of the egg, including the following:

Amount of moisture in the soil (ie, clay soil vs sandy soil)

Protection from direct sunlight (quickly kills eggs)

Temperatures of 5-34°C (41-93.2°F): A temperatures of 40°C (104°F) is lethal. A temperature of 38°C (68.4°F) is lethal after 8 days.

Soil humidity of more than 4%: The length of survival is 4.5 hours or less with soil humidity of less than 4%, varies at 4-50% soil humidity, and is best at more than 50% soil humidity

Formation of stage 2 larvae in the egg

Freezing at –15°C to –12°C (0.4-5°F) for 90 days kills all eggs except those at the single blastomere stage. Depth in the soil is another major influence. Experimentally, under similar climatic conditions, eggs survive 21–29 days on the surface, 1.5 years or less at a depth of 10-20 cm, and 2.5 years or less at a depth of 40-60 cm. Eggs and infective larva can survive over winter to infect in warmer weather. Under experimental conditions, eggs have survived for 6-14 years in the soil. However, in general, eggs are expected to survive 28-84 days. In areas of endemicity, particularly where night soil (human feces) or untreated wastewater is used as fertilizer, the egg concentration is 100 eggs per gram of soil. Eggs can be spread through the soil by earthworms, insects (eg, termites), and other burrowing animals. Egg-contaminated dust can be spread by wind and can lead to human infection via inhalation and swallowing.

In endemic areas eggs contaminate numerous domestic and public sites, including the following:
[2]

Chopping boards

Coins

Door handles

Dust

Fingers

Fingernail dirt

Fruit

Furniture

Insects

Nasal discharge

Paper money

Pickles

Public baths and restrooms

Public transportation (eg, buses)

Public squares (eg, sand, lawns)

School rooms

Underclothes

Vegetables

Wash basins

The average number of female offspring that attain reproductive capacity (reproductive number) produced by one adult female A lumbricoides worm is 1-6.

A lumbricoides and A suum

Evidence suggests that these parasites are separate species, although they are closely related. A lumbricoides infects humans almost exclusively and rarely infects pigs. A suum infects pigs almost exclusively and rarely infects humans. A lumbricoides has occasionally been reported in other animals, such as bears and primates, and A suum has occasionally been reported in cattle or sheep.

Morphologically, they are essentially indistinguishable; however, several reports cite differences in the denticles as a distinguishing characteristic. The morphology of the sex chromosomes exhibits differences, suggesting that the species are different. Species differences in the internal transcribed sequences of the ribosomal DNA have been reported, allowing differentiation. Protein profiles using 2-dimensional electrophoresis reveal reproducible differences. The current consensus is that these are, in fact, different species; however, they are closely related enough biologically that data on the life cycle and pathology of A suum have been extrapolated to humans.

Pathophysiological mechanism

Adult worms move throughout the GI tract and move in and out of orifices (eg, biliary tract, pancreas, appendix, diverticula, Meckel diverticulum) and may become incarcerated, leading to obstructive pathology. The worms may die, leading to inflammation, necrosis, infection, and abscess formation. If they migrate through an existing perforation in the bowel wall secondary to tuberculosis or typhoid, they can cause a granulomatous peritonitis. Larvae during migration may be deposited in the brain, spinal cord, kidney, or other organs, leading to granuloma formation, inflammation, or infection. They may become entwined in a bolus and obstruct the small bowel; this is most common in the terminal ileum, although other, more proximal, sites have been rarely reported.

This condition may be precipitated by the administration of an antihelminthic drug (see Medication). Eggs may be deposited in the liver or biliary tract. If they gain entry to the blood, they are deposited in extraneous sites, leading to local reactions.

Only a small percentage of Ascaris infections produce serious, acute pathology; however, because about one quarter of the human population is infected, the number of cases is significant.

Immunology

Humans make antibodies in response to Ascaris antigens and infection; immunoglobulin (Ig) E is predominant.
[3] The response is heterogeneous and is believed to confer some immunity. Evidence also suggests that whatever immunoprotection is conferred is not immunoglobulin-based.

Whether the presence of Ascaris infection increases risk or causes allergic disease or may have a protective effect remains controversial. Several studies demonstrate an association between Ascaris infection, seropositivity, or sensitization and allergic symptoms, sensitization, or asthma risk.
[4, 5, 6, 7] Some studies demonstrate a negative association.
[8, 9]

An association has been reported between egg excretion in children and increased prevalence of allergic disorders (eg, asthma) compared with children who do not excrete eggs. Because ascariasis and other helminthic infections are long-lived without producing consistently serious symptoms, a significant immunomodulatory relationship must occur between the infection and the human host, the details of which have not been fully clarified. Future research may lead to the development of vaccines and other interventions that will permit better control and treatment of this pervasive parasitic disease.

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Epidemiology

Frequency

United States

In the United States, more than 4 million individuals are believed to be infected with Ascaris species. Most infected persons are immigrants from developing countries, although the species are endemic in the southeastern United States in rural, low-income families.

During April 2010–March 2013, the Maine Department of Health and Human Services investigated multiple cases of ascariasis that had been reported by health-care providers, veterinarians, and patients. All of the cases were in persons who had lived or worked on Maine farms and had frequent exposure to pigs. After investigation, 14 persons on seven farms in Maine were identified with Ascaris infection.
[10]

International

Worldwide, more than 1.4 billion people are infected with ascariasis. The distribution of cases is as follows:

South America, Central America, and the Caribbean - 8.3%

Africa and the Middle East - 16.7%

Asia and the Oceania region - 75%

Ascariasis is present in at least 150 of the 218 countries in the world. Prevalence estimates widely vary among countries and within communities inside these countries.

Mortality/Morbidity

Annual mortality estimates range from 10,000-200,000. Currently, the rate is believed to be 10,000 deaths per year based on more detailed calculations.

Morbidity is proportional to the worm burden. A large majority of cases are asymptomatic. Intestinal obstruction, the most common complication of ascariasis, has been reported with as few as 4 worms. The average worm burden in numerous nonfatal case reports was 59 worms (range, 4-990); in fatal cases, the average worm burden was 659 (range, 23-1978).

Based on numerous reports in the literature, a rough estimate of the occurrence (percent of total complications) of complications is as follows:
[2]

A lumbricoides and other STHs have been shown to play a significant role in childhood malnutrition, which leads to growth retardation, cognitive impairment, and poor academic performance, resulting in a poorer quality of life and less ability to contribute to society. For the 3 major STHs, the disability-adjusted life years lost is 39 million years. Ascariasis accounts for 10.5 million years, hookworm infection accounts for 22.1 million years, and trichuriasis accounts for 6.4 million years. In comparison, malaria accounts for 35.7 million years.

Deworming with medications is one of many public health strategies to reduce infection rates and worm burden. Many studies demonstrate that after deworming, reinfection at the pretreatment level returns within 2-6 months, particularly, among the poor and socially disadvantaged. Several factors play a role in reinfection, including swimming in polluted rivers, absence of parent (at work) to supervise children, absence of toilet in house, running barefoot, eating without washing hands, geophagy (eating soil), eating unwashed fruits and vegetables, and chores that require contact with floors and ground.
[11, 12, 13]

Race

No racial predilection is recognized.

Sex

Hepatobiliary and pancreatic ascariasis (HPA) occurs with a greater frequency in women than men (76% in one series).
[14] In the same series, biliary surgery was more frequent in women (77%) and was an important risk factor for HPA. No other sex association is reported.

Age

Intestinal obstruction predominates in young children (85% of cases occur in children aged 1-5 y) but can occur at any age.

HPA is more common in adults than in children. In one large series of 500 patients, the age range was 4-70 years (median, 35 y).
[15]

Jones JL, Schulkin J, Maguire JH. Therapy for common parasitic diseases in pregnancy in the United States: a review and a survey of obstetrician/gynecologists' level of knowledge about these diseases. Obstet Gynecol Surv. 2005 Jun. 60(6):386-93. [Medline].

Contributor Information and Disclosures

Author

William H Shoff, MD, DTM&H Former Director, PENN Travel Medicine; Former Associate Professor, Department of Emergency Medicine, Hospital of the University of Pennsylvania, University of Pennsylvania School of Medicine